Show simple item record

Ecological and genetic interactions between cyanobacteria and viruses in a low‐oxygen mat community inferred through metagenomics and metatranscriptomics

dc.contributor.authorVoorhies, Alexander A.
dc.contributor.authorEisenlord, Sarah D.
dc.contributor.authorMarcus, Daniel N.
dc.contributor.authorDuhaime, Melissa B.
dc.contributor.authorBiddanda, Bopaiah A.
dc.contributor.authorCavalcoli, James D.
dc.contributor.authorDick, Gregory J.
dc.date.accessioned2017-06-16T20:09:39Z
dc.date.available2017-06-16T20:09:39Z
dc.date.issued2016-02
dc.identifier.citationVoorhies, Alexander A.; Eisenlord, Sarah D.; Marcus, Daniel N.; Duhaime, Melissa B.; Biddanda, Bopaiah A.; Cavalcoli, James D.; Dick, Gregory J. (2016). "Ecological and genetic interactions between cyanobacteria and viruses in a low‐oxygen mat community inferred through metagenomics and metatranscriptomics." Environmental Microbiology 18(2): 358-371.
dc.identifier.issn1462-2912
dc.identifier.issn1462-2920
dc.identifier.urihttps://hdl.handle.net/2027.42/137299
dc.publisherWiley Periodicals, Inc.
dc.publisherPRIMER‐E
dc.titleEcological and genetic interactions between cyanobacteria and viruses in a low‐oxygen mat community inferred through metagenomics and metatranscriptomics
dc.typeArticleen_US
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelMicrobiology and Immunology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/137299/1/emi12756-sup-0001-si.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/137299/2/emi12756.pdf
dc.identifier.doi10.1111/1462-2920.12756
dc.identifier.sourceEnvironmental Microbiology
dc.identifier.citedreferencePaez‐Espino, D., Morovic, W., Sun, C.L., Thomas, B.C., Ueda, K., Stahl, B., et al. ( 2013 ) Strong bias in the bacterial CRISPR elements that confer immunity to phage. Nat Commun 4: 1430.
dc.identifier.citedreferenceRobinson, J.T., Thorvaldsdottir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., and Mesirov, J.P. ( 2011 ) Integrative genomics viewer. Nat Biotechnol 29: 24 – 26.
dc.identifier.citedreferenceRodriguez‐Valera, F., Martin‐Cuadrado, A.‐B., Rodriguez‐Brito, B., Pasic, L., Thingstad, T.F., Rohwer, F., and Mira, A. ( 2009 ) Opinion: explaining microbial population genomics through phage predation. Nat Rev Microbiol 7: 828 – 836.
dc.identifier.citedreferenceRuberg, S.A., Kendall, S.T., Biddanda, B.A., Black, T., Nold, S.C., Lusardi, W.R., et al. ( 2008 ) Observations of the Middle Island Dinkhole in Lake Huron – a unique hydrogeologic and glacial creation of 400 million years. Mar Technol Soc J 42: 12 – 21.
dc.identifier.citedreferenceSamson, J.E., Magadan, A.H., Sabri, M., and Moineau, S. ( 2013 ) Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol 11: 675 – 687.
dc.identifier.citedreferenceSapranauskas, R., Gasiunas, G., Fremaux, C., Barrangou, R., Horvath, P., and Siksnys, V. ( 2011 ) The streptococcus thermophilus CRISPR/cas system provides immunity in Escherichia coli. Nucleic Acids Res 39: 9275 – 9282.
dc.identifier.citedreferenceSharon, I., Alperovitch, A., Rohwer, F., Haynes, M., Glaser, F., Atamna‐Ismaeel, N., et al. ( 2009 ) Photosystem I gene cassettes are present in marine virus genomes. Nature 461: 258 – 262.
dc.identifier.citedreferenceShi, Y., Tyson, G.W., and DeLong, E.F. ( 2009 ) Metatranscriptomics reveals unique microbial small RNAs in the ocean’s water column. Nature 459: 266 – 269.
dc.identifier.citedreferenceSorek, R., Kunin, V., and Hugenholtz, P. ( 2008 ) CRISPR – a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6: 181 – 186.
dc.identifier.citedreferenceStal, L.J. ( 2012 ) Cyanobacterial mats and stromatolites. In Ecology of Cyanobacteria II: Their Diversity in Space and Time. Whitton, B.A. (ed.). Heidelberg, Germany: Springer, pp. 65 – 125.
dc.identifier.citedreferenceSullivan, M.B., Lindell, D., Lee, J.A., Thompson, L.R., Bielawski, J.P., and Chisholm, S.W. ( 2006 ) Prevalence and evolution of core photosystem ii genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4: e234.
dc.identifier.citedreferenceSun, C.L., Barrangou, R., Thomas, B.C., Horvath, P., Fremaux, C., and Banfield, J.F. ( 2013 ) Phage mutations in response to CRISPR diversification in a bacterial population. Environ Microbiol 15: 463 – 470.
dc.identifier.citedreferenceTadmor, A.D., Ottesen, E.A., Leadbetter, J.R., and Phillips, R. ( 2011 ) Probing individual environmental bacteria for viruses by using microfluidic digital PCR. Science 333: 58 – 62.
dc.identifier.citedreferenceThingstad, T.F. ( 2000 ) Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 45: 1320 – 1328.
dc.identifier.citedreferenceTyson, G.W., and Banfield, J.F. ( 2008 ) Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10: 200 – 207.
dc.identifier.citedreferenceVoorhies, A.A., Biddanda, B.A., Kendall, S.T., Jain, S., Marcus, D.N., Nold, S.C., et al. ( 2012 ) Cyanobacterial life at low O 2: community genomics and function reveal metabolic versatility and extremely low diversity in a great lakes sinkhole mat. Geobiology 10: 250 – 267.
dc.identifier.citedreferenceWeinberger, A.D., Sun, C.L., Plucinski, M.M., Denef, V.J., Thomas, B.C., Horvath, P., et al. ( 2012 ) Persisting viral sequences shape microbial CRISPR‐based immunity. PLoS Comput Biol 8: e1002475.
dc.identifier.citedreferencevan der Westhuizen, A.J., and Eloff, J.N. ( 1985 ) Effect of temperature and light on the toxicity and growth of the blue‐green alga Microcystis aeruginosa (UV‐006). Planta 163: 55 – 59.
dc.identifier.citedreferenceYoshida, T., Nagasaki, K., Takashima, Y., Shirai, Y., Tomaru, Y., Takao, Y., et al. ( 2008 ) Ma‐lmm01 infecting toxic Microcystis aeruginosa illuminates diverse cyanophage genome strategies. J Bacteriol 190: 1762 – 1772.
dc.identifier.citedreferenceYoshida‐Takashima, Y., Yoshida, M., Ogata, H., Nagasaki, K., Hiroishi, S., and Yoshida, T. ( 2012 ) Cyanophage infection in the bloom‐forming Cyanobacteria Microcystis aeruginosa in surface freshwater. Microbes Environ 27: 350 – 355.
dc.identifier.citedreferenceZerbino, D.R., and Birney, E. ( 2008 ) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821 – 829.
dc.identifier.citedreferenceWeinbauer, M.G. ( 2004 ) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28: 127 – 181.
dc.identifier.citedreferenceAllers, E., Moraru, C., Duhaime, M.B., Beneze, E., Solonenko, N., Barrero‐Canosa, J., et al. ( 2013 ) Single‐cell and population level viral infection dynamics revealed by phagefish, a method to visualize intracellular and free viruses. Environ Microbiol 15: 2306 – 2318.
dc.identifier.citedreferenceAllwood, A.C., Walter, M.R., Kamber, B.S., Marshall, C.P., and Burch, I.W. ( 2006 ) Stromatolite reef from the Early Archaean era of Australia. Nature 441: 714 – 718.
dc.identifier.citedreferenceAnantharaman, K., Duhaime, M.B., Breier, J.A., Wendt, K.A., Toner, B.M., and Dick, G.J. ( 2014 ) Sulfur oxidation genes in diverse deep‐sea viruses. Science 344: 757 – 760.
dc.identifier.citedreferenceAnderson, M.J. ( 2001 ) A new method for non‐parametric multivariate analysis of variance. Austral Ecol 26: 32 – 46.
dc.identifier.citedreferenceAndersson, A.F., and Banfield, J.F. ( 2008 ) Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320: 1047 – 1050.
dc.identifier.citedreferenceAvrani, S., Wurtzel, O., Sharon, I., Sorek, R., and Lindell, D. ( 2011 ) Genomic island variability facilitates prochlorococcus–virus coexistence. Nature 474: 604 – 608.
dc.identifier.citedreferenceBanfield, J.F., and Young, M. ( 2009 ) Variety – the splice of life – in microbial communities. Science 326: 1198 – 1199.
dc.identifier.citedreferenceBarrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., et al. ( 2007 ) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709 – 1712.
dc.identifier.citedreferenceBiomatters ( 2013 ) Geneious. In.
dc.identifier.citedreferenceBogorad, L. ( 1975 ) Phycobiliproteins and complementary chromatic adaptation. Annu Rev Plant Physiol Plant Mol Biol 26: 369 – 401.
dc.identifier.citedreferenceBolhuis, H., and Stal, L.J. ( 2011 ) Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16s rRNA gene tag sequencing. ISME J 5: 1701 – 1712.
dc.identifier.citedreferenceBreitbart, M., Thompson, L.R., Suttle, C.A., and Sullivan, M.B. ( 2007 ) Exploring the vast diversity of marine viruses. Oceanography 20: 135 – 139.
dc.identifier.citedreferenceCai, F., Axen, S.D., and Kerfeld, C.A. ( 2013 ) Evidence for the widespread distribution of CRISPR‐cas system in the phylum Cyanobacteria. RNA Biol 10: 687 – 693.
dc.identifier.citedreferenceClarke, K., and Gorley, R.N. ( 2006 ) Primer v6: User Manual/Tutorial. Plymouth, UK: PRIMER‐E.
dc.identifier.citedreferenceClarke, K.R. ( 1993 ) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117 – 143.
dc.identifier.citedreferenceCollier, J.L., and Grossman, A.R. ( 1994 ) A small polypeptide triggers complete degradation of light‐harvesting phycobiliproteins in nutrient‐deprived cyanobacteria. EMBO J 13: 1039 – 1047.
dc.identifier.citedreferenceDammeyer, T., Bagby, S.C., Sullivan, M.B., Chisholm, S.W., and Frankenberg‐Dinkel, N. ( 2008 ) Efficient phage‐mediated pigment biosynthesis in oceanic cyanobacteria. Curr Biol 18: 442 – 448.
dc.identifier.citedreferenceDeng, L., Gregory, A., Yilmaz, S., Poulos, B.T., Hugenholtz, P., and Sullivan, M.B. ( 2012 ) Contrasting life strategies of viruses that infect photo‐ and heterotrophic bacteria, as revealed by viral tagging. Mbio 3: e00373‐12.
dc.identifier.citedreferenceDick, G.J., Andersson, A.F., Baker, B.J., Simmons, S.L., Yelton, A.P., and Banfield, J.F. ( 2009 ) Community‐wide analysis of microbial genome sequence signatures. Genome Biol 10: R85.
dc.identifier.citedreferenceEmerson, J.B., Thomas, B.C., Andrade, K., Allen, E.E., Heidelberg, K.B., and Banfield, J.F. ( 2012 ) Dynamic viral populations in hypersaline systems as revealed by metagenomic assembly. Appl Environ Microbiol 78: 6309 – 6320.
dc.identifier.citedreferenceFrias‐Lopez, J., Shi, Y., Tyson, G.W., Coleman, M.L., Schuster, S.C., Chisholm, S.W., and DeLong, E.F. ( 2008 ) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105: 3805 – 3810.
dc.identifier.citedreferenceGao, E.B., Gui, J.F., and Zhang, Q.Y. ( 2012 ) A novel cyanophage with a cyanobacterial nonbleaching protein a gene in the genome. J Virol 86: 236 – 245.
dc.identifier.citedreferenceGarcia‐Heredia, I., Martin‐Cuadrado, A.B., Mojica, F.J.M., Santos, F., Mira, A., Anton, J., and Rodriguez‐Valera, F. ( 2012 ) Reconstructing viral genomes from the environment using fosmid clones: the case of haloviruses. PLoS ONE 7: e33802.
dc.identifier.citedreferenceGarneau, J.E., Dupuis, M.E., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., et al. ( 2010 ) The CRISPR/cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468: 67 – 71.
dc.identifier.citedreferenceGilbert, J.A., Field, D., Huang, Y., Edwards, R., Li, W., Gilna, P., and Joint, I. ( 2008 ) Detection of large numbers of novel sequences in the metatranscriptomes of complex marine microbial communities. PLoS ONE 3: e3042.
dc.identifier.citedreferenceGiovannoni, S., Temperton, B., and Zhao, Y.L. ( 2013 ) Sar11 viruses and defensive host strains reply. Nature 499: E4 – E5.
dc.identifier.citedreferenceGolubic, S., and Abed, R. ( 2010 ) Entophysalis mats as environmental regulators. In Microbial Mats: Modern and Ancient Microorganisms in Stratified Systems. Seckbach, J., and Oren, A. (eds). Dordrecht, The Netherlands: Springer, pp. 239 – 251.
dc.identifier.citedreferenceGrissa, I., Vergnaud, G., and Pourcel, C. ( 2007a ) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8: 172.
dc.identifier.citedreferenceGrissa, I., Vergnaud, G., and Pourcel, C. ( 2007b ) CRISPFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35: W52 – W57.
dc.identifier.citedreferenceGuindon, S., and Gascuel, O. ( 2003 ) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696 – 704.
dc.identifier.citedreferenceHaft, D.H., Selengut, J., Mongodin, E.F., and Nelson, K.E. ( 2005 ) A guild of 45 CRISPR‐associated (cas) protein families and multiple CRISPR/cas subtypes exist in prokaryotic genomes. PLoS Comput Biol 1: 474 – 483.
dc.identifier.citedreferenceHeidelberg, J.F., Nelson, W.C., Schoenfeld, T., and Bhaya, D. ( 2009 ) Germ warfare in a microbial mat community: CRISPRs provide insights into the co‐evolution of host and viral genomes. PLoS ONE 4: e4169.
dc.identifier.citedreferenceHendrix, R.W., Smith, M.C.M., Burns, R.N., Ford, M.E., and Hatfull, G.F. ( 1999 ) Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc Natl Acad Sci USA 96: 2192 – 2197.
dc.identifier.citedreferenceHoehler, T.M., Bebout, B.M., and Des Marais, D.J. ( 2001 ) The role of microbial mats in the production of reduced gases on the early earth. Nature 412: 324 – 327.
dc.identifier.citedreferenceHorvath, P., and Barrangou, R. ( 2010 ) CRISPR/cas, the immune system of bacteria and archaea. Science 327: 167 – 170.
dc.identifier.citedreferenceHurwitz, B.L., and Sullivan, M.B. ( 2013 ) The pacific ocean virome (pov): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS ONE 8: e57355.
dc.identifier.citedreferenceHurwitz, B.L., Hallam, S.J., and Sullivan, M.B. ( 2013 ) Metabolic reprogramming by viruses in the sunlit and dark ocean. Genome Biol 14: R123.
dc.identifier.citedreferenceHyatt, D., Chen, G.‐L., LoCascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. ( 2010 ) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
dc.identifier.citedreferenceIgnacio‐Espinoza, J.C., and Sullivan, M.B. ( 2012 ) Phylogenomics of t4 cyanophages: lateral gene transfer in the ‘core’ and origins of host genes. Environ Microbiol 14: 2113 – 2126.
dc.identifier.citedreferenceKarradt, A., Sobanski, J., Mattow, J., Lockau, W., and Baier, K. ( 2008 ) Nbla, a key protein of phycobilisome degradation, interacts with clpc, a hsp100 chaperone partner of a cyanobacterial clp protease. J Biol Chem 283: 32394 – 32403.
dc.identifier.citedreferenceKashtan, N., Roggensack, S.E., Rodrigue, S., Thompson, J.W., Biller, S.J., Coe, A., et al. ( 2014 ) Single‐cell genomics reveals hundreds of coexisting subpopulations in wild prochlorococcus. Science 344: 416 – 420.
dc.identifier.citedreferenceKristensen, D.M., Waller, A.S., Yamada, T., Bork, P., Mushegian, A.R., and Koonin, E.V. ( 2013 ) Orthologous gene clusters and taxon signature genes for viruses of prokaryotes. J Bacteriol 195: 941 – 950.
dc.identifier.citedreferenceLi, H., and Durbin, R. ( 2009 ) Fast and accurate short read alignment with burrows–wheeler transform. Bioinformatics 25: 1754 – 1760.
dc.identifier.citedreferenceLi, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., et al. ( 2009 ) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078 – 2079.
dc.identifier.citedreferenceLindell, D., Sullivan, M.B., Johnson, Z.I., Tolonen, A.C., Rohwer, F., and Chisholm, S.W. ( 2004 ) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 101: 11013 – 11018.
dc.identifier.citedreferenceLindell, D., Jaffe, J.D., Johnson, Z.I., Church, G.M., and Chisholm, S.W. ( 2005 ) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438: 86 – 89.
dc.identifier.citedreferenceLitchman, E. ( 2000 ) Growth rates of phytoplankton under fluctuating light. Freshw Biol 44: 223 – 235.
dc.identifier.citedreferenceLitchman, E., Steiner, D., and Bossard, P. ( 2003 ) Photosynthetic and growth responses of three freshwater algae to phosphorus limitation and daylength. Freshw Biol 48: 2141 – 2148.
dc.identifier.citedreferenceLiu, X., Kong, S., Shi, M., Fu, L., Gao, Y., and An, C. ( 2008 ) Genomic analysis of freshwater cyanophage pf‐wmp3 infecting cyanobacterium Phormidium foveolarum: the conserved elements for a phage. Microb Ecol 56: 671 – 680.
dc.identifier.citedreferenceLuque, I., and Forchhammer, K. ( 2008 ) Nitrogen assimilation and c/n balance sensing. In The Cyanobacteria: Molecular Biology, Genomics, and Evolution. Herrero, A., and Flores, E. (eds). Norfolk, UK: Caister Academic Press, pp. 335 – 382.
dc.identifier.citedreferenceLuque, I., Zabulon, G., Contreras, A., and Houmard, J. ( 2001 ) Convergence of two global transcriptional regulators on nitrogen induction of the stress‐acclimation gene nbla in the Cyanobacterium synechococcus sp pcc 7942. Mol Microbiol 41: 937 – 947.
dc.identifier.citedreferenceMa, Y., Paulsen, I.T., and Palenik, B. ( 2012 ) Analysis of two marine metagenomes reveals the diversity of plasmids in oceanic environments. Environ Microbiol 14: 453 – 466.
dc.identifier.citedreferenceMakarova, K.S., Grishin, N.V., Shabalina, S.A., Wolf, Y.I., and Koonin, E.V. ( 2006 ) A putative RNA‐interference‐based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1: 7.
dc.identifier.citedreferenceMakarova, K.S., Aravind, L., Wolf, Y.I., and Koonin, E.V. ( 2011a ) Unification of cas protein families and a simple scenario for the origin and evolution of CRISPR‐cas systems. Biol Direct 6: 38.
dc.identifier.citedreferenceMakarova, K.S., Haft, D.H., Barrangou, R., Brouns, S.J.J., Charpentier, E., Horvath, P., et al. ( 2011b ) Evolution and classification of the CRISPR‐cas systems. Nat Rev Microbiol 9: 467 – 477.
dc.identifier.citedreferenceMann, N.H., Cook, A., Millard, A., Bailey, S., and Clokie, M. ( 2003 ) Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424: 741.
dc.identifier.citedreferenceMiddelboe, M. ( 2000 ) Bacterial growth rate and marine virus–host dynamics. Microb Ecol 40: 114 – 124.
dc.identifier.citedreferenceMizuno, C.M., Rodriguez‐Valera, F., Kimes, N.E., and Ghai, R. ( 2013 ) Expanding the marine virosphere using metagenomics. PLoS Genet 9: e1003987.
dc.identifier.citedreferenceNamiki, T., Hachiya, T., Tanaka, H., and Sakakibara, Y. ( 2012 ) MetaVelvet: an extension of velvet assembler to de novo metagenome assembly from short sequence reads. Nucleic Acids Res 40: e155.
dc.identifier.citedreferencevan der Oost, J., Jore, M.M., Westra, E.R., Lundgren, M., and Brouns, S.J.J. ( 2009 ) CRISPR‐based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci 34: 401 – 407.
dc.identifier.citedreferencePride, D.T., and Schoenfeld, T. ( 2008 ) Genome signature analysis of thermal virus metagenomes reveals archaea and thermophilic signatures. BMC Genomics 9: 420.
dc.identifier.citedreferencePride, D.T., Sun, C.L., Salzman, J., Rao, N., Loomer, P., Armitage, G.C., et al. ( 2011 ) Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res 21: 126 – 136.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.